The repair of skeletal muscle requires iron recycling through macrophage ferroportin

Journal of Immunology

Volumn 197, Issue 5, 2016, Pages 1914-1925

  Corna, Gianfranca ^a   Caserta, Imma ^a,b   Monno, Antonella ^a   Apostoli, Pietro ^c   Manfredi, Angelo A ^a,b   Camaschella, Clara ^a,b   Rovere Querini, Patrizia ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c UNIVERSITY OF BRESCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CD163 ANTIGEN; CELL PROTEIN; FERRITIN; FERRITIN H; FERROPORTIN; FPN PROTEIN; HEME OXYGENASE 1; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; CATION TRANSPORT PROTEIN; CELL SURFACE RECEPTOR; DIFFERENTIATION ANTIGEN; HEME; IRON; LEUKOCYTE ANTIGEN; METAL TRANSPORTING PROTEIN 1; TRANSFERRIN;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CELL INFILTRATION; CELL ISOLATION; CHEMICAL PARAMETERS; CONTROLLED STUDY; FEMALE; HOMEOSTASIS; IRON HOMEOSTASIS; IRON RECYCLING; IRON STORAGE; LIPID STORAGE; MACROPHAGE; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE REGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SKELETAL MUSCLE; TISSUE DEGENERATION; UPREGULATION; ADIPOSE TISSUE; ANIMAL; CHEMISTRY; CYTOLOGY; DEFICIENCY; GENETICS; IMMUNOLOGY; METABOLISM; MUSCLE FIBRIL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; REGENERATION; WOUND HEALING;

ADIPOSE TISSUE; ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CATION TRANSPORT PROTEINS; HEME; HEME OXYGENASE-1; HOMEOSTASIS; IRON; MACROPHAGES; MICE; MUSCLE, SKELETAL; MYOFIBRILS; RECEPTORS, CELL SURFACE; REGENERATION; TRANSFERRIN; WOUND HEALING;

EID: 84983748392     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501417     Document Type: Article

References (54)

1. Arnold, L., A. Henry, F. Poron, Y. Baba-Amer, N. van Rooijen, A. Plonquet, R. K. Gherardi, and B. Chazaud. 2007. Inflammatory monocytes recruited after skeletal muscle injury switch into antiinflammatory macrophages to support myogenesis. J. Exp. Med. 204: 1057-1069.
2. Bosurgi, L., G. Corna, M. Vezzoli, T. Touvier, G. Cossu, A. A. Manfredi, S. Brunelli, and P. Rovere-Querini. 2012. Transplanted mesoangioblasts require macrophage IL-10 for survival in a mouse model of muscle injury. J. Immunol. 188: 6267-6277.
3. Warren, G. L., T. Hulderman, D. Mishra, X. Gao, L. Millecchia, L. O'Farrell, W. A. Kuziel, and P. P. Simeonova. 2005. Chemokine receptor CCR2 involvement in skeletal muscle regeneration. FASEB J. 19: 413-415.
4. Ruffell, D., F. Mourkioti, A. Gambardella, P. Kirstetter, R. G. Lopez, N. Rosenthal, and C. Nerlov. 2009. A CREB-C/EBPbeta cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc. Natl. Acad. Sci. USA 106: 17475-17480.
5. Sciorati, C., E. Rigamonti, A. A. Manfredi, and P. Rovere-Querini. 2016. Cell death, clearance and immunity in the skeletal muscle. Cell Death Differ. 23: 927-937.
6. Deng, B., M. Wehling-Henricks, S. A. Villalta, Y. Wang, and J. G. Tidball. 2012. IL-10 triggers changes in macrophage phenotype that promote muscle growth and regeneration. J. Immunol. 189: 3669-3680.
7. Corna, G., L. Campana, E. Pignatti, A. Castiglioni, E. Tagliafico, L. Bosurgi, A. Campanella, S. Brunelli, A. A. Manfredi, P. Apostoli, et al. 2010. Polarization dictates iron handling by inflammatory and alternatively activated macrophages. Haematologica 95: 1814-1822.
8. Gaetano, C., L. Massimo, and M. Alberto. 2010. Control of iron homeostasis as a key component of macrophage polarization. Haematologica 95: 1801-1803.
9. Bories, G., S. Colin, J. Vanhoutte, B. Derudas, C. Copin, M. Fanchon, M. Daoudi, L. Belloy, S. Haulon, C. Zawadzki, et al. 2013. Liver X receptor activation stimulates iron export in human alternative macrophages. Circ. Res. 113: 1196-1205.
10. Pantopoulos, K., S. K. Porwal, A. Tartakoff, and L. Devireddy. 2012. Mechanisms of mammalian iron homeostasis. Biochemistry 51: 5705-5724.
11. Kawane, K., H. Fukuyama, G. Kondoh, J. Takeda, Y. Ohsawa, Y. Uchiyama, and S. Nagata. 2001. Requirement of DNase II for definitive erythropoiesis in the mouse fetal liver. Science 292: 1546-1549.
12. Knutson, M. D., M. Oukka, L. M. Koss, F. Aydemir, and M. Wessling-Resnick. 2005. Iron release from macrophages after erythrophagocytosis is up-regulated by ferroportin 1 overexpression and down-regulated by hepcidin. Proc. Natl. Acad. Sci. USA 102: 1324-1328.
13. Ganz, T. 2012. Macrophages and systemic iron homeostasis. J. Innate Immun. 4: 446-453.
14. Beaumont, C., and C. Delaby. 2009. Recycling iron in normal and pathological states. Semin. Hematol. 46: 328-338.
15. Andrews, N. C., and P. J. Schmidt. 2007. Iron homeostasis. Annu. Rev. Physiol. 69: 69-85.
16. Bratosin, D., J. Mazurier, J. P. Tissier, J. Estaquier, J. J. Huart, J. C. Ameisen, D. Aminoff, and J. Montreuil. 1998. Cellular and molecular mechanisms of senescent erythrocyte phagocytosis by macrophages. A review. Biochimie 80: 173-195.
17. Guillaud, C., V. Loustau, and M. Michel. 2012. Hemolytic anemia in adults: main causes and diagnostic procedures. Expert Rev. Hematol. 5: 229-241.
18. Delaby, C., N. Pilard, H. Puy, and F. Canonne-Hergaux. 2008. Sequential regulation of ferroportin expression after erythrophagocytosis in murine macrophages: early mRNA induction by haem, followed by iron-dependent protein expression. Biochem. J. 411: 123-131.
19. Marro, S., D. Chiabrando, E. Messana, J. Stolte, E. Turco, E. Tolosano, and M. U. Muckenthaler. 2010. Heme controls ferroportin1 (FPN1) transcription involving Bach1, Nrf2 and a MARE/ARE sequence motif at position-7007 of the FPN1 promoter. Haematologica 95: 1261-1268.
20. Camaschella, C. 2013. Iron and hepcidin: a story of recycling and balance. Hematology Am. Soc. Hematol. Educ. Program 2013: 1-8.
21. Hentze, M. W., M. U. Muckenthaler, B. Galy, and C. Camaschella. 2010. Two to tango: regulation of mammalian iron metabolism. Cell 142: 24-38.
22. Beard, J. L. 2001. Iron biology in immune function, muscle metabolism and neuronal functioning. J. Nutr. 131: 568S-579S; discussion 580S.
23. Vezzoli, M., P. Castellani, G. Corna, A. Castiglioni, L. Bosurgi, A. Monno, S. Brunelli, A. A. Manfredi, A. Rubartelli, and P. Rovere-Querini. 2011. Highmobility group box 1 release and redox regulation accompany regeneration and remodeling of skeletal muscle. Antioxid. Redox Signal. 15: 2161-2174.
24. Cordani, N., V. Pisa, L. Pozzi, C. Sciorati, and E. Clementi. 2014. Nitric oxide controls fat deposition in dystrophic skeletal muscle by regulating fibroadipogenic precursor differentiation. Stem Cells 32: 874-885.
25. Santambrogio, P., A. Cozzi, S. Levi, E. Rovida, F. Magni, A. Albertini, and P. Arosio. 2000. Functional and immunological analysis of recombinant mouse H-and L-ferritins from Escherichia coli. Protein Expr. Purif. 19: 212-218.
26. Tidball, J. G., and S. A. Villalta. 2010. Regulatory interactions between muscle and the immune system during muscle regeneration. Am. J. Physiol. Regul. Integr. Comp. Physiol. 298: R1173-R1187.
27. Kohyama, M., W. Ise, B. T. Edelson, P. R. Wilker, K. Hildner, C. Mejia, W. A. Frazier, T. L. Murphy, and K. M. Murphy. 2009. Role for Spi-C in the development of red pulp macrophages and splenic iron homeostasis. Nature 457: 318-321.
28. Robertson, T. A., M. A. Maley, M. D. Grounds, and J. M. Papadimitriou. 1993. The role of macrophages in skeletal muscle regeneration with particular reference to chemotaxis. Exp. Cell Res. 207: 321-331.
29. McLennan, I. S. 1996. Degenerating and regenerating skeletal muscles contain several subpopulations of macrophages with distinct spatial and temporal distributions. J. Anat. 188: 17-28.
30. Tidball, J. G. 2002. Interactions between muscle and the immune system during modified musculoskeletal loading. Clin. Orthop. Relat. Res. 403(Suppl.): S100-S109.
31. St Pierre, B. A., and J. G. Tidball. 1994. Differential response of macrophage subpopulations to soleus muscle reloading after rat hindlimb suspension. J. Appl. Physiol. 77: 290-297.
32. Chazaud, B., C. Sonnet, P. Lafuste, G. Bassez, A. C. Rimaniol, F. Poron, F. J. Authier, P. A. Dreyfus, and R. K. Gherardi. 2003. Satellite cells attract monocytes and use macrophages as a support to escape apoptosis and enhance muscle growth. J. Cell Biol. 163: 1133-1143.
33. Warren, G. L., L. O'Farrell, M. Summan, T. Hulderman, D. Mishra, M. I. Luster, W. A. Kuziel, and P. P. Simeonova. 2004. Role of CC chemokines in skeletal muscle functional restoration after injury. Am. J. Physiol. Cell Physiol. 286: C1031-C1036.
34. Summan, M., G. L. Warren, R. R. Mercer, R. Chapman, T. Hulderman, N. Van Rooijen, and P. P. Simeonova. 2006. Macrophages and skeletal muscle regeneration: a clodronate-containing liposome depletion study. Am. J. Physiol. Regul. Integr. Comp. Physiol. 290: R1488-R1495.
35. Tidball, J. G., and M. Wehling-Henricks. 2007. Macrophages promote muscle membrane repair and muscle fibre growth and regeneration during modified muscle loading in mice in vivo. J. Physiol. 578: 327-336.
36. Segawa, M., S. Fukada, Y. Yamamoto, H. Yahagi, M. Kanematsu, M. Sato, T. Ito, A. Uezumi, S. Hayashi, Y. Miyagoe-Suzuki, et al. 2008. Suppression of macrophage functions impairs skeletal muscle regeneration with severe fibrosis. Exp. Cell Res. 314: 3232-3244.
37. Lu, H., D. Huang, N. Saederup, I. F. Charo, R. M. Ransohoff, and L. Zhou. 2011. Macrophages recruited via CCR2 produce insulin-like growth factor-1 to repair acute skeletal muscle injury. FASEB J. 25: 358-369.
38. Brigitte, M., C. Schilte, A. Plonquet, Y. Baba-Amer, A. Henri, C. Charlier, S. Tajbakhsh, M. Albert, R. K. Gherardi, and F. Chrétien. 2010. Muscle resident macrophages control the immune cell reaction in a mouse model of notexininduced myoinjury. Arthritis Rheum. 62: 268-279.
39. Sindrilaru, A., T. Peters, S. Wieschalka, C. Baican, A. Baican, H. Peter, A. Hainzl, S. Schatz, Y. Qi, A. Schlecht, et al. 2011. An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J. Clin. Invest. 121: 985-997.
40. Goodnough, J. B., E. Ramos, E. Nemeth, and T. Ganz. 2012. Inhibition of hepcidin transcription by growth factors. Hepatology 56: 291-299.
41. Ono, Y., F. Calhabeu, J. E. Morgan, T. Katagiri, H. Amthor, and P. S. Zammit. 2011. BMP signalling permits population expansion by preventing premature myogenic differentiation in muscle satellite cells. Cell Death Differ. 18: 222-234.
42. Haldar, M., M. Kohyama, A. Y. So, W. Kc, X. Wu, C. G. Briseño, A. T. Satpathy, N. M. Kretzer, H. Arase, N. S. Rajasekaran, et al. 2014. Heme-mediated SPI-C induction promotes monocyte differentiation into iron-recycling macrophages. Cell 156: 1223-1234.
43. Sciorati, C., E. Clementi, A. A. Manfredi, and P. Rovere-Querini. 2015. Fat deposition and accumulation in the damaged and inflamed skeletal muscle: cellular and molecular players. Cell. Mol. Life Sci. 72: 2135-2156.
44. Yamauchi, T., and T. Kadowaki. 2013. Adiponectin receptor as a key player in healthy longevity and obesity-related diseases. Cell Metab. 17: 185-196.
45. Kawai, M., and C. J. Rosen. 2010. PPARg: a circadian transcription factor in adipogenesis and osteogenesis. Nat. Rev. Endocrinol. 6: 629-636.
46. Garner, B., K. Roberg, and U. T. Brunk. 1998. Endogenous ferritin protects cells with iron-laden lysosomes against oxidative stress. Free Radic. Res. 29: 103-114.
47. Orino, K., L. Lehman, Y. Tsuji, H. Ayaki, S. V. Torti, and F. M. Torti. 2001. Ferritin and the response to oxidative stress. Biochem. J. 357: 241-247.
48. Joe, A.W., L. Yi, A. Natarajan, F. Le Grand, L. So, J.Wang, M. A. Rudnicki, and F. M. Rossi. 2010. Muscle injury activates resident fibro/adipogenic progenitors that facilitate myogenesis. Nat. Cell Biol. 12: 153-163.
49. Uezumi, A., S. Fukada, N. Yamamoto, S. Takeda, and K. Tsuchida. 2010. Mesenchymal progenitors distinct from satellite cells contribute to ectopic fat cell formation in skeletal muscle. Nat. Cell Biol. 12: 143-152.
50. Huang, P., T. J. Schulz, A. Beauvais, Y. H. Tseng, and E. Gussoni. 2014. Intramuscular adipogenesis is inhibited by myo-endothelial progenitors with functioning Bmpr1a signalling. Nat. Commun. 5: 4063.
51. Zumbrennen-Bullough, K. B., Q. Wu, A. B. Core, S. Canali, W. Chen, I. Theurl, D. Meynard, and J. L. Babitt. 2014. MicroRNA-130a is up-regulated in mouse liver by iron deficiency and targets the bone morphogenetic protein (BMP) receptor ALK2 to attenuate BMP signaling and hepcidin transcription. J. Biol. Chem. 289: 23796-23808.
52. Ahmadian, M., J. M. Suh, N. Hah, C. Liddle, A. R. Atkins, M. Downes, and R. M. Evans. 2013. PPARg signaling and metabolism: the good, the bad and the future. Nat. Med. 19: 557-566.
53. Duan, S. Z., C. Y. Ivashchenko, M. W. Russell, D. S. Milstone, and R. M. Mortensen. 2005. Cardiomyocyte-specific knockout and agonist of peroxisome proliferator-activated receptor-gamma both induce cardiac hypertrophy in mice. Circ. Res. 97: 372-379.
54. Son, N. H., T. S. Park, H. Yamashita, M. Yokoyama, L. A. Huggins, K. Okajima, S. Homma, M. J. Szabolcs, L. S. Huang, and I. J. Goldberg. 2007. Cardiomyocyte expression of PPARgamma leads to cardiac dysfunction in mice. J. Clin. Invest. 117: 2791-2801.